RUNX2 tandem repeats and the evolution of facial length in placental mammals

BMC Evolutionary Biology

Brenda J Bradley²  Robert J Asher¹  Nicholas I Mundy¹  Frédéric Delsuc⁵  Stephen G B Chester²  Vera Warmuth¹  Jason M Kamilar³  Marie A Pointer⁴ 

[1] Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK;Department of Anthropology, Yale University, New Haven, Connecticut 06511, USA;School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona 85287, USA;Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK;Institut des Sciences de l'Evolution, UMR5554-CNRS-IRD, Université Montpellier II, Montpellier, France

关键词: Morphology;    Xenarthra;    Afrotheria;    Primates;    Molecular evolution;    Prognathism;    Mammalian evolution;   

Others  :  1140961
DOI  :  10.1186/1471-2148-12-103

 received in 2012-01-12, accepted in 2012-06-28,  发布年份 2012

【 摘 要 】

Background

When simple sequence repeats are integrated into functional genes, they can potentially act as evolutionary ‘tuning knobs’, supplying abundant genetic variation with minimal risk of pleiotropic deleterious effects. The genetic basis of variation in facial shape and length represents a possible example of this phenomenon. Runt-related transcription factor 2 (RUNX2), which is involved in osteoblast differentiation, contains a functionally-important tandem repeat of glutamine and alanine amino acids. The ratio of glutamines to alanines (the QA ratio) in this protein seemingly influences the regulation of bone development. Notably, in domestic breeds of dog, and in carnivorans in general, the ratio of glutamines to alanines is strongly correlated with facial length.

Results

In this study we examine whether this correlation holds true across placental mammals, particularly those mammals for which facial length is highly variable and related to adaptive behavior and lifestyle (e.g., primates, afrotherians, xenarthrans). We obtained relative facial length measurements and RUNX2 sequences for 41 mammalian species representing 12 orders. Using both a phylogenetic generalized least squares model and a recently-developed Bayesian comparative method, we tested for a correlation between genetic and morphometric data while controlling for phylogeny, evolutionary rates, and divergence times. Non-carnivoran taxa generally had substantially lower glutamine-alanine ratios than carnivorans (primates and xenarthrans with means of 1.34 and 1.25, respectively, compared to a mean of 3.1 for carnivorans), and we found no correlation between RUNX2 sequence and face length across placental mammals.

Conclusions

Results of our diverse comparative phylogenetic analyses indicate that QA ratio does not consistently correlate with face length across the 41 mammalian taxa considered. Thus, although RUNX2 might function as a ‘tuning knob’ modifying face length in carnivorans, this relationship is not conserved across mammals in general.

【 授权许可】

   
2012 Pointer et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1 .

Figure 2 .

Figure 3 .

【 参考文献 】

• [1]Nadeau N, Jiggins C: Golden age for evolutionary genetics? Genomic studies of adaptation in natural populations. Trends Genet 2011, 26:484-492.
• [2]Grenier CS, Scott JW: From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. 2nd edition. Wiley-Blackwell, Oxford; 2004.
• [3]Hoekstra HE: Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 2006, 97:222-234.
• [4]Wagner GP, Lynch VJ: The gene regulatory logic of transcription factor evolution. Trends Ecol Evol 2008, 23:377-385.
• [5]Kashi Y, King DG: Simple sequence repeats as advantageous mutators in evolution. Trends Genet 2006, 22:253-259.
• [6]Haerty W, Golding GB: Genome-wide evidence for selection acting on single amino acid repeats. Genome 2010, Research 20:755-760.
• [7]Wren JD, Forgacs E, Fondon JW, Pertsemlidis A, Cheng SY, et al.: Repeat polymorphisms within gene regions: Phenotypic and evolutionary implications. Am J Hum Genet 2000, 67:345-356.
• [8]Caburet S, Cocquet J, Vaiman D, Veitia RA: Coding repeats and evolutionary "agility". Bioessays 2005, 27:581-587.
• [9]Karlin S, Burge C: Trinucleotide repeats and long homopeptides in genes and roteins associated with nervous system disease and development. Proc Natl Acad Sci USA 1996, 93:1560-1565.
• [10]Alba MM, Guigo R: Comparative analysis of amino acid repeats in rodents and humans. Genome Res 2004, 14:549-554.
• [11]Fondon JW, Garner HR: Molecular origins of rapid and continuous morphological evolution. Proc Natl Acad Sci USA 2004, 101:18058-18063.
• [12]Fondon JW, Garner HR: Detection of length-dependent effects of tandem repeat alleles by 3-D geometric decomposition of craniofacial variation. Dev Genes Evol 2007, 217:79-85.
• [13]Sears KE, Goswami A, Flynn JJ, Niswander LA: The correlated evolution of Runx2 tandem repeats, transcriptional activity, and facial length in Carnivora. Evol Dev 2007, 9:555-565.
• [14]Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, et al.: Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997, 89:765-771.
• [15]Ziros PG, Basdra EK, Papavassiliou AG: Runx2: of bone and stretch. Int J Biochem Cell Biol 2008, 40:1659-1663.
• [16]Thirunavukkarasu K, Mahajan M, McLarren KW, Stifani S, Karsenty G: Two domains unique to osteoblast-specific transcription factor Osf2/Cbfa1 contribute to its transactivation function and its inability to heterodimerize with Cbf beta. Mol Cell Biol 1998, 18:4197-4208.
• [17]Zhou G, Chen Y, Zhou L, Thirunavukkarasu K, Hecht J, et al.: CBFA1 mutation analysis and functional correlation with phenotypic variability in cleidocranial dysplasia. Hum Mol Genet 1999, 8:2311-2316.
• [18]Mundlos S: Cleidocranial dysplasia: clinical and molecular genetics. J Med Genet 1999, 36:177-182.
• [19]Asher RJ, Lehmann T: Dental eruption in afrotherian mammals. BMC Biol 2008, 6:14. BioMed Central Full Text
• [20]Komori T: Regulation of bone development and maintenance by Runx2. Front Biosci 2008, 13:898-903.
• [21]Green R, Krause J, Briggs A, Maricic T, Stenzel U, et al.: A Draft Sequence of the Neandertal Genome. Science 2010, 710-722.
• [22]King DG, Soller M, Kashi Y: Evolutionary tuning knobs. Endeavour 1997, 21:36-40.
• [23]Nowak R: Walker's Mammals of the World. 6th edition. Johns Hopkins Univ Press, Baltimore; 1999.
• [24]Delsuc F, Vizcaino SF, Douzery EJP: Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans. BMC Evol Biol 2004, 4.
• [25]Möller-Krull M, Delsuc F, Churakov G, et al.: Retroposed elements and their flanking regions resolve the evolutionary history of xenarthran mammals (armadillos, anteaters, and sloths). Mol Biol Evol 2007, 24:2573-2582.
• [26]Asher RJ, Maree S, Bronner G, Bennett NC, Bloomer P, et al.: A phylogenetic estimate for golden moles (Mammalia, Afrotheria, Chrysochloridae). BMC Evol Biol 2010, 10:69. BioMed Central Full Text
• [27]Asher RJ, Bennett N, Lehmann T: The new framework for understanding placental mammal evolution. Bioessays 2009, 31:853-864.
• [28]Lartillot N, Poujol R: A phylogenetic model for investigating correlated evolution of substitution rates and continuous phenotypic characters. Mol Biol Evol 2011, 28:729-744.
• [29]Greenwood AD, Castresana J, Feldmaier-Fuchs G, Paabo S: A molecular phylogeny of two extinct sloths. Mol Phylogenet Evol 2001, 18:94-103.
• [30]Galant R, Carroll SB: Evolution of a transcriptional repression domain in an insect Hox protein. Nature 2002, 415:910-913.
• [31]Quader S, Isvaran K, Hale RE, Miner BG, Seavy NE: Nonlinear relationships and phylogenetically independent contrasts. J Evol Biol 2004, 17:709-715.
• [32]Banovich NE, Ritzman TB, Stone AC: The Runx2 gene is an important determinant of facial morphology in primates. Am J Phys Anthropol 2011, 144:81-81.
• [33]1000 Genomes Browserwww.1000genomes.org webcite
• [34]Kaessmann H, Wiebe V, Weiss G, Pääbo S: Great ape DNA sequences reveal a reduced diversity and an expansion in humans. Nat Genet 2001, 27:155-156.
• [35]Singleton M: Patterns of cranial shape variation in the Papionini (Primates : Cercopithecinae). J Hum Evol 2002, 42:547-578.
• [36]Fleagle JG, Gilbert CC, Baden AL: Primate Cranial Diversity. Am J Phys Anthropol 2010, 142:565-578.
• [37]Richtsmeier JT, Weiss KM, Buchanan A, Walker A, Jablonski N, et al.: Developmental genetic basis of primate craniofacial variation and human origins. Am J Phys Anthropol 2007, 140:198.
• [38]Willmore RCKE, Rogers J, Richtsmeier JT, Cheverud JM: Genetic variation in baboon craniofacial sexual dimorphism. Evolution 2009, 63:799-806.
• [39]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Molecular Biology 1990, 215:403-410.
• [40]Neanderthal Genome Browserhttp://genome.ucsc.edu/Neandertal/ webcite
• [41]Catzeflis FM: Animal tissue collections for molecular genetics and Systematics. Trends Ecolology and Evolution 1991, 6:168.
• [42]Janis CM: Correlation of cranial and dentail variables with body size in ungulates and macropodoids. In Body size in mammalian paleobiology: estimation and biological implications. Edited by Damuthand J, MacFadden BJ. Cambridge University Press, New York; 1990:255-298.
• [43]Fitch WT: Skull dimensions in relation to body size in nonhuman primates: the causal bases for acoustic allometry. Zoology 2000, 103:40-58.
• [44]Freckleton RP: The seven deadly sins of comparative analysis. J Evol Biol 2009, 22:1367-1375.
• [45]Felsenstein J: Phylogenies and the comparative method. Am Nat 1985, 125:1-15.
• [46]Pagel M: Inferring the historical patterns of biological evolution. Nature 1999, 401:877-884.
• [47]Rohlf FJ: Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution 2001, 55:2143-2160.
• [48]Cooper N, Freckleton RP, Jetz W: Phylogenetic conservatism of environmental niches in mammals. Proceedings of the Royal Society B-Biological Sciences 2011, 278:2384-2391.
• [49]Kamilar JM, Bradley BJ: Interspecific variation in primate coat color supports Gloger’s rule. J Biogeogr 2011, 38:2270-2277.
• [50]Heesy CP, Kamilar JM, Willms J: Retinogeniculostriate pathway components scale with orbit convergence only in primates and not in other mammals. Brain Behav Evol 2011, 77:105-115.
• [51]Orme CDL, Freckleton RP, Thomas GH, Petzoldt T, Fritz SA, Isaac NJB: Comparative Analyses of Phylogenetics and Evolution in R. 2011. R package version 0.4
• [52]R Development Core Team: R: A Language And Environment For Statistical Computing. R Foundation for Statistical Computing, Vienna; 2007.
• [53]Quinn G, Keough M: Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge; 2002.
• [54]Arnold C, Matthews LJ, Nunn CL: The 10k Trees Website: A New Online Resource for Primate Phylogeny. Evolutionary Anthropology 2010, 19:114-118.
• [55]Hallstrom BM, Janke A: Resolution among major placental mammal interordinal relationships with genome data imply that speciation influenced their earliest radiations. BMC Evol Biol 2008, 8:162. BioMed Central Full Text
• [56]Poux C, Madsen O, Glos J, de Jong WW, Vences M: Molecular phylogeny and divergence times of Malagasy tenrecs: Influence of data partitioning and taxon sampling on dating analyses. BMC Evol Biol 2008, 8:102. BioMed Central Full Text
• [57]Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Back RMD, et al.: The delayed rise of present-day mammals. Nature 2007, 446:507-512.
• [58]Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, et al.: The delayed rise of present-day mammals (vol 446, pg 507, 2007). Nature 2008, 456:274-274.
• [59]Eizirik E, Murphy WJ, Koepfli KP, Johnson WE, Dragoo JW, et al.: Pattern and timing of diversification of the mammalian order Carnivora inferred from multiple nuclear gene sequences. Mol Phylogenet Evol 2010, 56:49-63.
• [60]Benton MJ, Donoghue PCJ, Asher RJ: Calibrating and constraining molecular clocks. In Timetree of Life. Edited by Hedges KSSB. Oxford University Press; 2009:35-86.
• [61]Dryad Repositoryhttp://dx.doi.org/10.5061/dryad.fr84hd25 webcite